Effect of oxygen conditions on intracapsular development in two calyptraeid species with different modes of larval development

Abstract

Oxygen availability in the aggregation of offspring has been shown to be a critical factor affecting the survival and development of embryos in aquatic systems. It is not yet known, however, to what extent the capacity to provide O 2 to embryo aggregations may act on the time of parental protection (here encapsulation), ultimately determining indirect and direct embryonic development. We assessed O 2 conditions during encapsulation, the factors determining those conditions, and the consequences on embryo survival in 2 gastropod species with contrasting developmental modes: Crepidula fornicata, an indirect developer, and Crepidula coquimbensis, a direct developer showing adelphophagy. Results showed that intracapsular O 2 conditions decreased to almost hypoxic conditions throughout development in C. fornicata, in contrast to the oxygenated conditions observed in C. coquimbensis during the entire encapsulation period. These contrasting patterns between species were explained by: (1) differences in metabolic rate of the embryos, (2) differences in total metabolizing material per capsule throughout development, and (3) differences in wall thickness and rates of decay throughout development, which may affect O 2 diffusion. Moreover, when the low O 2 conditions observed at the end of the encapsulation period were maintained after hatching by artificially extending encapsulation for 3 d, a dramatic negative effect on embryonic survival was observed in the indirect developer. In contrast, no effect on juvenile survival was observed in the direct developer. We suggest that hatching at intermediate stages of embryonic development in C. fornicata may be a response to increased O 2 constraints during the encapsulated period. KEY WORDS: Parental protection · Oxygen limitation · Developmental mode · Larvae · Crepidula · EncapsulationResale or republication not permitted without written consent of the publisher Mar Ecol Prog Ser 368: 197-207, 2008 aggregation in jelly masses or capsules to active guarding of the embryos by the parents (Pechenik 1979, Rumrill 1990. A wide range of physical factors can also influence offspring development and survival, determining the need for parental protection, affecting its extent, and ultimately driving its evolution (Williams 1966, Trivers 1972, Clutton-Brock 1991, Roff 2002. In aquatic systems, the low solubility and diffusion rate of O 2 in water seem to be major constraints of parental protection through offspring aggregation (in amphibians: Crump 1996; in marine invertebrates: Booth 1995, Cohen & Strathmann 1996, Dick et al. 1998, Lee & Strathmann 1998, Fernández et al. 2000. Embryo aggregations of marine invertebrate species exhibit low O 2 levels which negatively affect embryonic development and survival (Strathmann & Strathmann 1982, Chaffee & Strathmann 1984, Strathmann & Chaffee 1984, Cancino et al. 2000. However, the consequences of reduced development and mortality risks during the protected phase on the optimal time of parental protection in aquatic systems are sti...

Limiting factors to encapsulation: the combined effects of dissolved protein and oxygen availability on embryonic growth and survival of species with contrasting feeding strategies

“…Protection against desiccation, osmotic changes, UV or predation are some of the numerous advantages of this strategy (for a review, see Przeslawski, 2004). In spite of the advantages of embryo packing in aquatic systems, encapsulated embryos must confront two important constraints during development: food and oxygen limitations (Pechenik, 1979;Strathmann and Stranthmann, 1995;Brante et al, 2008). The consequences of these constraints on species showing embryos with different feeding strategies are poorly understood.…”

Differences in the timing of cardio-respiratory development determine whether marine gastropod embryos survive or die in hypoxia

“…Comparisons with previous studies where isolated gastropod eggs or embryos were exposed to chronic hypoxia show a general concordance with the impacts on growth, development and survival that we observed in L. obtusata (but see discussion of velum plasticity below). Only around 1 in 10 eggs of the slipper limpet, Crepidula fornicata, survived a 3 day exposure to an environmental P O2 of 3.2 kPa (Brante et al, 2008) and no embryos of the nassarid Nassarius festivus hatched successfully when cultured in seawater of P O2 of just less than 1 kPa (Chan et al, 2008). It should be noted that both these P O2 values are considerably lower than we used in our study.…”

“…However, there is also evidence of negative effects even at P O2 values similar to those we used (8 kPa), which may not be classified by ecologists as being environmental hypoxia (Vaquer-Sunyer and Duarte, 2008). While the survival of the encapsulated slipper limpet, C. coquimbensis, was not significantly affected by exposure to P O2 of ∼11.5 kPa (Brante et al, 2008), Brante et al (2009) later found that aerobic metabolism of embryos of this species and the related C. fornicata decreased significantly at P O2 <12 kPa. Similarly, development, hatching and shell secretion of the encapsulated muricid snail Chorus giganteus were all compromised by culture in seawater of P O2 ∼10 kPa (Cancino et al, 2003(Cancino et al, , 2011 and embryonic development of N. festivus was significantly delayed when cultured at a P O2 of ∼7.6 kPa (Chan et al, 2008).…”

“…Low P O2 is a common feature within egg masses of gastropods and is induced by respiration of embryos (Chaffee and Strathmann, 1984;Brante et al, 2008;Cancino et al, 2011). Levels of hypoxia often vary throughout the mass, with consequences for embryonic development.…”

Kinship and the evolution of social behaviours in the sea

“…Indeed, encapsulation engenders some of the most extreme forms of parent-offspring conflict and sibling rivalry, including consumption of non-developing nurse eggs (oophagy) and of viable siblings (adelphophagy) [34]. Siblings not only compete for nutrients provided by their parents, but also for resources that are affected by the packaging per se, such as the availability of oxygen [35,36]. The ubiquity of egg masses, capsules and other forms of encapsulation in marine invertebrates suggests that competition among siblings occurs frequently.…”